Effects of Seawater Acidification on Echinoid Adult Stage: History
View Latest Version
Please note this is an old version of this entry, which may differ significantly from the current revision.
Contributor:
Davide Asnicar
,
Maria Gabriella Marin

The continuous release of CO2 in the atmosphere is increasing the acidity of seawater worldwide, and the pH is predicted to be reduced by ~0.4 units by 2100. Ocean acidification (OA) is changing the carbonate chemistry, jeopardizing the life of marine organisms, and in particular calcifying organisms. Because of their calcareous skeleton and limited ability to regulate the acid–base balance, echinoids are among the organisms most threatened by OA.

  • ocean acidification
  • echinoids
  • sea urchin
  • physiology

1. Introduction

The usage of fossil fuels and deforestation are constantly emitting carbon dioxide (CO2) into the atmosphere, increasing its concentration [1]. This is recognized to be the most important factor causing climate change. Oceans play an important role in mitigating the greenhouse effect caused by CO2 [2]. They have absorbed around 30–40% of the anthropogenic carbon dioxide [3][4], making the effects on land and the atmosphere milder but threatening marine organisms. Higher temperature and deoxygenation are causing the migration of animals towards other, more suitable environments, causing disruptions at the community level. Other climate change drivers are sneakier, and harder for animals to avoid. The increase in CO2 absorbed by the ocean, due to the disruption of the carbonate system and the increase in H+ in seawater [5], is slowly but steadily lowering the pH of the marine environment worldwide, causing ocean acidification (OA), which represents a problem to the marine biota [1][6][7]. Models (Intergovernmental Panel on Climate Change—IPCC, Representative Concentration Pathway RCP8.5) predict that the pH value of surface seawater will decrease by ~0.4 units by the end of this century if the CO2 emissions continue in a “business-as-usual” scenario [1][8].
OA effects on marine biota have been studied broadly in the past decade, highlighting interspecific variability in the response to this stressor [9][10][11][12][13]. Different animals have different sensitivities towards stressors due to physiological, behavioural and reproductive differences, even within closely related groups [14][15]. For example, gut pH regulation was shown to differ in six Ambulacraria species and was correlated with different sensitivity to OA. In particular, the species with the best ability to regulate pH were the most sensitive towards acidification conditions in terms of both survival and growth [9].
Calcifying organisms are especially threatened by acidification, due to the reduction in calcium carbonate (CaCO3) saturation and, therefore, bioavailability [7]. For example, the mortality rate of oceanic copepods increased by 50% when animals were exposed to a reduction of 0.2 pH units [16]. However, the range of tolerance to pH variations and calcium carbonate bioavailability can vary among calcifers. Echinoderms have a calcareous skeleton mainly constituted of aragonite and calcite (CaCO3 crystal forms) with a high magnesium calcite (MgCO3) content [17]. MgCO3 solubility is higher than CaCO3, resulting in increased vulnerability of echinoderms to OA [18][19]. This is particularly evident in the Echinoidea class since sea urchins are highly calcified.
Because of their important role as a keystone species and their high sensitivity and rapid response to environmental changes, echinoids have been extensively used as model species in ecology and ecotoxicology studies to assess the effects of different stressors in the context of climate change and pollution [20][21][22].

2. SWA Effects on Echinoid Calcification

The mineralogical composition of sea urchins varies greatly among species, but also among individuals and among different structures of each individual [23]. In most echinoids, approximately 4% calcite has magnesium ions that substitute calcium ions. Mg-calcite is more soluble than calcite and therefore, in relation to the high Mg content, the skeletal structures of echinoids are especially weakened in a more acidic environment [17][23][24][25][26]. The Mg-calcite content of sea urchin skeletal structures, and therefore their solubility in acidified conditions, vary with latitude, being higher in warmer waters [23]. In all the collected studies concerning test skeletal mineralogy and the related ability to tolerate mechanical stress, 7 out of 12 species showed alterations due to low pH. Alterations were detected in both short-term and long-term exposure.
S. virgulata, exposed at a pH reduced by 0.4 and 0.6 units [27], after 14 days had less calcite and lost weight. S. droebachiensis instead showed traces of carbonate dissolution after 42 days, but only at the greatest ΔpH (0.81 compared with control) [28]. In the other four species subjected to longer exposures (from 56 days up to being resident in vent systems), low pH conditions did not cause a variation in the calcification. Only one case of long exposure (146 days) to reduced pH resulted in decreased mechanical properties of the T. gratilla skeleton. The force needed to break the sea urchin test was lower if animals were maintained at low pH compared with those at pH 8.1. However, the effect of SWA was significant only if the ΔpH was −0.5 units, and not in the case of 0.3 [29].
Alterations in calcification were present also in animals resident in CO2 vents. Differences in the element composition were found in P. lividus and A. lixula specimens sampled in volcanic vent systems in the Mediterranean Sea. In particular, in the test of animals sampled in three acidified sites (ΔpH 0.36, 0.61 and 0.63 compared with the control site, pH 8.11), manganese and strontium contents were significantly higher, whereas zinc content was significantly lower [30]. Those specimens also suffered higher skeletal degradation with microfractures visible using scanning electron microscopy. Species-specific differences were found, with more severe effects in P. lividus than A. lixula [30]. However, the effect of local variability is a key point that must be considered in the response of calcification to SWA. Indeed, a similar study performed in another volcanic vent system in the Mediterranean Sea (local pH 7.63, reduced by 0.3 units compared with the control site) showed that A. lixula was more sensitive to SWA than P. lividus. Alterations in the gene expression were associated with decreased mechanical properties of the spines and test in A. lixula [31]. Nonetheless, in both studies, A. lixula maintained higher abundance in the vent sites compared with P. lividus [30][31]. This suggested that other factors were involved in the maintenance of the populations (e.g., larval plasticity influencing the settlement).
The duration of exposure to SWA has major relevance to the occurrence of skeletal mineralogy changes. This suggests that echinoids can maintain active calcification processes, making the carbonate bioavailability stable [32]. In addition, SWA effects are negligible in the case that the ΔpH is smaller than 0.4, and are usually more severe when ΔpH is greater than 0.4 units. For example, the sea urchin S. variolaris kept for 210 days at a pH reduced by 0.2 units did not show effects on the skeletal mineralogy and the spine integrity. However, if specimens were kept at a pH reduction of 0.5 units, the skeletal characteristics varied significantly compared with the control [33]. In the study of Dery and colleagues, traces of corrosion were highlighted in Eucidaris tribuloides exposed to pH 7.4 for 45 days, whereas no effects were observed at pH 7.7 [34]. Several experiments demonstrated that the prolongation of the exposure can lead to an improvement in the condition, resulting in a decreased acidification impact. The reduction in calcium carbonate saturation in seawater can be compensated for by modulating gene expression, as reported by Emerson and colleagues [35]. Indeed, Lytechinus variegatus exposed to pH 7.7 and 7.47 for 56 days showed impairment in the development of spines but the genes involved in the regeneration process were upregulated. This suggested that, with time, those animals would have been able to face SWA [35].
The difficulty of building calcareous structures in an acidified environment can lead to impairment in the growth of the skeletal parts of echinoids (test, jaws, and spines). This was the case for S. droebachiensis [28] and P. lividus [36] maintained at a pH reduced by 0.34–0.81 units for the former, and 0.2–0.5 units for the latter, for 42 and 60 days, respectively. An impairment of the growth was also found in a T. gratilla aquaculture system with a high density of individuals and a scarce seawater change [37]. Indeed, this led to a reduction in the pH in the tanks with an output similar to ocean acidification. The growth of H. erythrogramma and Echinometra spp., instead, was not impaired by low pH conditions, either in a laboratory exposure [38][39][40], or in animals collected in a vent system [41].
As seen above, echinoids can counteract the adverse effects of environmental acidification on calcification through compensatory mechanisms; however, the overall skeletal mechanical properties may be compromised. For example, in T. gratilla maintained for 146 days at pH 8.1–7.8–7.6, the mineralogy of the skeleton did not vary, but the force needed to break the skeleton was significantly lower [29], possibly due to alteration of the structure. On the other hand, P. lividus resident in a vent system had the same mineral composition as the outside-vent animals [42], and the force applied to break the skeleton was not significantly different in acidic and not-acidic conditions [43]. Similarly, the mechanical properties (i.e., resistance to perforation and compression, fracture force, and test stiffness) of P. lividus exposed to pH 7.9 and 7.8 for 360 days were not different from those of the control at pH 8.1 [43]. The last two examples, in contrast with that found by Byrne and colleagues [29], suggest again that the longer the exposure, the better the response of sea urchins to reduced pH. However, T. gratilla and P. lividus have different growth rates, being faster in the former species. This condition can make T. gratilla more susceptible to SWA, as it needs to deposit more calcium carbonate in less time, with negative consequences on the mechanical properties of calcareous structures. Moreover, the skeletal structure’s degradation has been correlated with changes in the accumulation of essential and non-essential metals in P. lividus and A. lixula resident in CO2-vent systems [30].
Whether or not the echinoids are able to maintain the calcification rate, they may face a cost [44], as also seen for other calcifers [45]. Indeed, other physiological processes are impacted by SWA and these may be more relevant to study than the calcification processes. Increased CO2 concentration in seawater is associated with hypercapnia (i.e., an abnormal increase in CO2 partial pressure in organisms) and oxygen loss [1]. This condition may generate stress, suppressing organisms’ metabolism [46] and compromising processes such as behaviour and reproduction [47][48][49].

3. SWA Effects on Echinoid Physiology

The increase in CO2 concentration can impair the ion exchange between extra- and intra-cellular environments, inducing acidosis [50], which, in cascade, can lead to metabolic alterations [51]. Most relevant effects associated with hypercapnia include (i) metabolism alteration, (ii) modification of the tissue acid–base regulation, (iii) reduced rates of protein synthesis, (iv) increase in oxygen consumption and ventilation rate, and (v) enhanced production of adenosine in nervous tissue, potentially inducing behavioural depression [49][52].
Echinoderms are considered hypometabolic, since they show low respiratory rates and are not efficient in balancing the concentration of ions in their extracellular fluids [46]. Their metabolism is influenced not only by the size and nutritional state but also by several environmental parameters, such as seasonality, oxygen tension, water temperature, salinity and pH [46][53][54]. Therefore, in sea urchins, the coelomic fluid pH might be strongly influenced by environmental pH, as they show a very low or partial compensation capability [53][55]. However, from the literature survey, the coelomic fluid of the Echinoidea seems to respond well to SWA. In 61% of the papers where the coelomic fluid pH was assessed, no differences were found between animals maintained at low and natural pH. The buffering capacity is maintained for animals from the equatorial to the temperate regions. Stumpp and colleagues [56] suggested that two strategies can be adopted against environmentally induced acidosis: HCO3− accumulation to compensate for acid–base disruption or proton extrusion mediated through NH4+ excretion.
Another effect of hypercapnia is the increase in the concentration of reactive oxygen species in animal tissues [57], thus inducing the organism to increase antioxidant defence mechanisms in order to diminish the oxidative damage. Both short- and long-term exposures showed the induction of stress-related enzymatic activities in the animal tissues [27][42][58] and no oxidative damage was observed (although oxidative damage was assessed only in animals resident in CO2 vents [42]). Overall, the antioxidant capacity seems to be efficient in maintaining the homeostasis of the animals, even though the effects of hypercapnia have been observed in the acid–base regulation.
The acid–base balance is, indeed, one of the endpoints that are the most influenced by the pH reduction. The three sea urchin species P. lividus, T. ventricosus and E. mathaei showed the regulation of the dissolved inorganic carbon (DIC) and alkalinity to maintain the pH level in the coelomic fluid [40][59][60], even if exposure conditions were not the same. In another experiment carried out with P. lividus by Cohen-Rengifo and colleagues [36], the exposure for 60 days at a pH reduction of 0.2 and 0.5 did not cause a modification in the acid–base regulation. In addition, the pH of the coelomic fluid and the respiration rate of those animals were not altered, suggesting the acclimation of P. lividus for those endpoints at least [36]. This was confirmed by the work of Marčeta and colleagues [58] where P. lividus maintained for 60 days at pH 8.1, 7.7 and 7.4 showed no significant variations in respiration, ammonia excretion rates and assimilation efficiency [58]. In a shorter-term experiment (19 days), at pH 8.1, 7.7 and 7.4, P. lividus showed evidence of stress resulting in a coelomic fluid pH reduction and a respiration rate increase [55]. In particular, the oxygen uptake of P. lividus maintained at 10 °C at seawater pH levels of 7.7 and 7.4 was significantly higher compared with the control [55]. However, differences were not present in the experimental groups maintained at 16 °C, suggesting that the response observed varies depending on the interaction of both pH and temperature. Indeed, it is known that respiration and metabolic rates can change with temperature as well as other biological aspects, such as feeding activities [61][62][63]. Other environmental stressors instead may exacerbate SWA negative effects. Indeed, antioxidant capacity alteration was found in P. lividus specimens maintained in copper-spiked (0.1 µM) water at a pH reduced by 0.4 units, with additive effects due to the combination of high pCO2 and contaminant [59]. Thus, future studies need to use a multiple-stressor approach in order to understand how echinoids will respond to future climate change scenarios.
Metabolic modifications linked to high pCO2 have been reported in both marine vertebrates [64] and invertebrates, but in the latter group, the effects are more evident, considering their poor ability to regulate extracellular pH [49][52][65]. In fact, in organisms such as molluscs, corals and echinoderms, a decrease in seawater pH is often associated with elevated metabolic rates, since more energy to maintain homeostasis [66] and carbonate structures is required [47]. Respiration and nitrogen excretion are useful tools to assess the physiological status of an organism and have been used as such for decades [67]. The ratio between the oxygen consumed and the nitrogen excreted indicates the level of activity of oxidative and protein metabolism [67][68]. Moreover, O/N has been used as an index of stress related to variations in biotic and abiotic factors, such as reproductive cycle, food quality and availability, temperature, dissolved oxygen, salinity and pollution [68][69].
Results about ammonia excretion and respiration rates are summarized. Contrary to expectations, for both endpoints, minimal effects of pH or acclimation to this driver have been reported. Only a few studies showed effects linked to low pH exposure, mostly in short-term experiments that lasted a few weeks [53][55][56][70]. In adult sea urchins of Strongylocentrotus droebachiensis exposed to very low pH levels (7.60–7.16) for 45 days, the rate of NH4+ excretion was significantly higher [56] compared with the control at pH 8.01. Since the respiration rate did not change significantly in sea urchins maintained at low pH conditions, the oxygen:nitrogen atomic ratio was significantly lower [56], suggesting that the catabolism of proteins was prevalent compared with the catabolism of lipids and carbohydrates [68]. Similarly, P. lividus specimens maintained at pH 7.6 for 180 days showed a significantly higher ammonia excretion rate in the trials carried out after 60 and 90 days of exposure. In the following trials, instead, the values were no more significantly different from the control at pH 8.0 [71]. However, the importance of local biological adaptation was highlighted by Asnicar et al. [71] where two groups of sea urchins with different ecological backgrounds were used. The group that experienced more environmental variability was shown to be more resilient and able to acclimate to SWA sooner than the other group. S. neumayeri maintained for 40 months at a pH reduced by 0.26 and 0.46 units showed an increase in respiration rate and energy consumption at the lowest pH value tested [72]. However, the overall somatic and reproductive growth were not impaired. This suggests that animals may take time to acclimate to low pH conditions and that this time-frame may differ among the various species and even within the same species. H. erythrogramma specimens maintained at pH 7.6 for two months showed an increase in the oxygen uptake rate, compared with the control condition. Respiration was even enhanced in the exposure combination of pH 7.6 and +5 °C temperature [53]. Despite this boost in respiration rate, the feeding rate (a proxy of the ability to obtain energetic resources) was not affected by the tested SWA condition. If higher energy demand is not accompanied by higher energy uptake, somatic growth and gonad development may be compromised. This would eventually result in weaker and smaller sea urchins that could be more threatened by abiotic and biotic challenges. However, in the studies considered, sea urchin size was not affected by low pH [35][73].
Interestingly, the endpoints summarized here under the category “Food intake”showed more alterations in the long-term exposures (e.g., [70][74][75]) than in the short-term ones (e.g., [53][60][73]). As reported by Wang and colleagues [70], physiological responses might be time-dependent, with differences among the various endpoints considered.
Sea urchins were demonstrated to be able to acclimate their metabolism even under low pH conditions, if enough time is given to them. Indeed, animals sampled in a naturally acidified site (the volcanic vent site in Ischia), and therefore exposed to SWA conditions throughout their whole life, have a similar metabolism to other sea urchins sampled outside the vent site [42].
Lastly, the immune system of the sea urchins showed the ability to acclimatize to seawater acidification, but the response is species-specific. Short-term exposure (5 days) of L. variegatus and E. lucunter to pH 7.6 and 7.3 revealed the initial depression of the immunity capacity with a lowered number of haemocytes and their reduced phagocytic activity [76]. However, in another study, after an initial disruption, the recovery of the immune system was shown in S. droebachiensis after 7 days of exposure to a reduction of 0.5 pH units. No signs of disruption or depression were detected in the P. lividus immune system, when resident in CO2 vents [42][77].

4. SWA Effects on Echinoid Behaviour

There is evidence that SWA also affects animals’ behaviour. The literature is still sparse, although growing fast [64][78][79][80][81]. Linked to extracellular acidosis, the altered ion gradient across the neural membrane induces membrane depolarization, neural pathway excitation and ultimately an altered behaviour [48][82]. As stated above, hypercapnia and low pH may also promote the enhanced production of adenosine in nervous tissue, which can result in behavioural alteration [49][52]. Both invertebrates and vertebrates can be influenced [78], although the impact of SWA on vertebrate behaviour seems to be weak [64][83] compared with invertebrate responses [80]. SWA effects on invertebrate behaviour have been explored in many taxa, among which are the echinoids, and the results show a range of negative, neutral or positive responses [80]. It must be taken into account that the magnitude of changes in behaviour, in the context of future SWA scenarios, seems to be species-specific and varies depending upon the ecosystem and the particular behaviour considered.
In the literature collected in the present review, only 10 experiments investigated the effects of SWA on the behaviour of echinoids. Among the 24 endpoints considered, 10 were altered by lower pH. Considering the ecological relevance of sea urchins’ behavioural traits, it is increasingly important to assess their modifications in relation to environmental stressors. Behavioural changes may lead to remarkable effects on the animal’s fitness and at the community or the ecosystem level [61][84][85][86]. Considering behaviours such as feeding and predator avoidance, SWA can affect the population and community structure. The effects can be direct on sea urchins or indirect on their food source. For example, the exposure of the deep-sea echinoid Strongylocentrotus fragilis to a −0.46 pH reduction caused an increase in the foraging time [87]. On the other hand, the exposure of the algae Ulva lactuca to high pCO2 (4000 µ-atm) resulted in an increase in unpalatable substances and the consequent decrease in grazing on the algae by the sea urchin T. gratilla [88]. The calcifying algae Halimeda incrassata significantly reduced its calcium carbonate content and therefore reduced its defence against grazers L. variegatus and Diadema antillarum [89]. Interestingly, in the work of Burnham and colleagues [73], the exposure of the sea urchin L. variegatus to a −0.3 units pH reduction for 42 days caused an alteration of the animals’ feeding habits, but if the algae were also exposed to low pH, the sea urchins’ preferences returned similar to those of the control [73]. Therefore, predictions about the balance between vegetation and foragers for the future are difficult and further investigation is required.
The righting is the action that a sea urchin executes to return to its natural aboral side-up position after a displacement in an inverse position [90]. A quick righting is linked to good physiological status, as it requires good coordinating capacities between the spines and tube feet [91], while changes in righting time are related to stress [92]. The covering behaviour consists of taking ambient elements (small rocks, shells or algae) with the tube feet to cover the aboral surface [93][94]. Sea urchin righting, covering and shelter-seeking behaviours enable the animal to escape from predators, reach crevices or seagrass meadows, prevent the occlusion of the apical openings of the water vascular system (madreporite) and seek protection from solar radiation and physical turbulence [95][96][97][98][99][100]. Investigating the possible impacts of acidification on behavioural endpoints could help to predict the sea urchins’ responses in an acidification scenario as ecosystem engineers. A decrease in their reactions would lead to a major exposure to predators and radiation, and difficulties in finding food or reaching conspecifics for reproduction. It has been demonstrated that the exposure to low pH for 3 months led to a decrease in predator-avoidance behaviour of the sea urchin P. lividus [101]. This, together with the reduction in defensive capacity (i.e., thinner plates and spines weakness [101]) may compromise survival chance, with cascading effects on the benthic community.
Due to its simplicity, the righting response is the most common endpoint analysed in research aimed at evaluating sea urchin stress. The righting time was not impaired in P. lividus exposed for 60 or 180 days to a pH reduction of 0.3,0.4 and 0.6 units [58][71] and in L. variegatus exposed for 42 days to pH 7.60 (control pH 7.97) [73], or for 56 days to pH 7.7–7.47 (control pH 7.93) [35]. Among the research that investigated the righting response, this endpoint was significantly increased only in one case. Specimens of S. fragilis were exposed to three scenarios, with the pH reduced by 0.28, 0.69 and 1.31 units compared with the natural condition. The impairment in the righting response was significant in the two lowest pHs, which are extreme values with little relevance for near-future scenarios [74].
The shelter-seeking behaviour in relation to environmental stressors has been poorly studied [102][103][104] and was assessed under reduced pH conditions in only one experiment [71]. The experiment considered the shelter-seeking response to SWA of two sea urchin populations, both exposed for 180 days. Specimens were collected within a highly variable environment (the Lagoon of Venice) and in a coastal area, more stable in terms of physico-chemical characteristics. The two populations responded differently to the low pH condition. The shelter-seeking behaviour of lagoonal animals was impaired only slightly, particularly in the first months of exposure. Instead, the response of animals from the other site was affected by low pH, with a reduction in the number of sheltered sea urchins, distance travelled and animal speed. The lagoonal group managed to acclimate to low pH towards the end of the exposure, while the other did not [71]. Future studies should consider the shelter-seeking behaviour together with the righting, as the former might be a more sensitive endpoint.
Although it was investigated in one experiment only [36], the resistance to induced water flow seems to be another sensitive endpoint to consider. The dislodgment of P. lividus specimens subjected to a strong water flow was easier at low pH (7.7–7.4), suggesting lower adhesive strength in the tube feet [36]. For animals living close to the surface in the subtidal area or in intertidal pools, this would entail a greater risk of predation and the need to return quickly to a natural position. Nasuchon and colleagues [105] found that exposure to high pCO2 levels for 48 days caused a change in the proteomic profile of the tube feet in Pseudocentrotus depressus, resulting in reduced contraction force and weakened adhesion and therefore movement impairment. This was not confirmed in P. lividus exposed at pH 7.7 and 7.4 for 56 days, since the characteristics of the tube feet (extensibility, strength, stiffness and toughness) were similar to those in controls, suggesting that other biological features might be involved in the behavioural alteration [36].

5. SWA Effects on Echinoid Reproduction

In the present work, data concerning SWA effects on reproduction at the parental level were collected, and gonadal development, gonadal quality and female fecundity (i.e., number of eggs released) were considered.
The sea urchin S. virgulata exposed for 14 days to reduced pH showed lesions on the oocytes at pH 7.8 and 7.6 [27]. Gonads of S. neumayeri exposed to pH 7.8 and 7.6 for 30 days showed an increase in tissue damage, neoplasia and oocyte lesions [106]. The gonadal development of males of Echinometra sp. was delayed when animals were maintained for 70 days at pH 7.9 [32]. As seen for the previous endpoints considered, the longer the exposure, the more similar the results are between low-pH and control sea urchins (e.g., [107]). This was not the case for H. pulcherrimus maintained at pH 7.83 for 270 days, which showed a delay of one month in the development of the gonads compared with the control at pH 8.1 [75]. To explain this result, a reduction in food intake was hypothesized. Nonetheless, the female fecundity did not change between pH levels, suggesting that the delay was functional. The development delay may entail two detrimental effects: (i) delay of the spawning event to a less favourable period of the reproductive season; and (ii) occurrence of a spawning event with eggs in a lower amount or of lower quality. Both cases lead to unknown consequences for the filial generation, which may have to cope with unfavourable physico-chemical conditions and predation. In another experiment, Hazan and colleagues exposed Echinometra sp. specimens to pH 8.1 and 7.7 and checked the gonad status monthly for 330 days. The gonadal index and maturation at pH 7.7 were not different compared with the control [108]. The exposure of Echinometra sp. was longer than that experienced by H. pulcherrimus [75], but even considering the same time of exposure under experimental conditions, in the former case the gonadal maturation was not delayed under the SWA scenario.
In T. gratilla, the gonadal index, expressed as the ratio of gonad weight to animal weight, revealed significantly smaller gonads in specimens kept at low pH (7.8 and 7.6) for 146 days [109]. Although animals were fed ad libitum, even their total body weight was lower at reduced pH, but not significantly. A similar outcome was found in the work by Mos and colleagues [37], where T. gratilla was cultured in high density and the biogenic production of CO2 led to effects similar to SWA with a reduction in gonad production. However, in this case, a reduction in somatic growth was also documented, after 42 days of exposure at pH 7.8 and 7.6. Overall, these results suggest that only after longer exposure to reduced pH, as in the work of Dworjanyn and Byrne [109], do sea urchins shift energy from gonadal to somatic growth. Similarly, Echinometra sp. sampled in a CO2 volcanic vent system (pH 7.48) had smaller gonads compared with the control site specimens [41]. Interestingly, this was the only negative effect of pH noticed in the work of Uthicke and colleagues. As for the other parameters considered in that study, animals from the vents performed better than their counterparts at pH 8.0. Indeed, after a 17-month monitoring period, the average growth of the animals was significantly higher at the vent site [41].
Female fecundity is an important endpoint to consider in order to understand if a shift in energy allocation happened. As seen in the paragraph concerning SWA effects on physiology, the disruption of metabolism and therefore the reallocation of resources towards survival and growth rather than reproduction might take place in a short–medium-term exposure. This trend can change with the prolongation of the exposure, reallocating energy towards reproduction, as observed in S. droebachiensis exposed to pH 7.7 in a long-term exposure [107]. Indeed, the number of eggs released by a female was significantly lower after 120 days of exposure, but it was no longer different from control conditions (pH 8.1) after 480 days of exposure. The researchers concluded that after 480 days, animals were fully acclimated to the low pH and were able to use the energy stored to develop eggs, since they did not need it for other biological necessities [107].
Other aspects linked to reproduction success may be affected by SWA, enlarging the variety of endpoints to be studied. Many papers explored the effects of reduced pH on gametes, fertilization success, embryo and larval quality and fitness. In external fertilizers, SWA may have an important effect due to the limited buffering capacity of internal pH in sperm [110]. To achieve fertilisation, sperm are subjected to intense selection and competition, as only a small proportion will succeed in fertilizing an egg [111] and selection will favour high-quality ejaculate [112].

This entry is adapted from the peer-reviewed paper 10.3390/jmse10040477

References

  1. Pörtner, H.-O.; Roberts, D.C.; Masson-Delmotte, V.; Zhai, P.; Tignor, M.; Poloczanska, E.; Mintenbeck, K.; Alegría, A.; Nicolai, M.; Okem, A.; et al. (Eds.) IPCC 2019 Special Report on the Ocean and Cryosphere in a Changing Climate; Cambridge University Press: Cambridge, UK; New York, NY, USA, 2019; 755p.
  2. Le Quéré, C.; Raupach, M.R.; Canadell, J.G.; Marland, G.; Bopp, L.; Ciais, P.; Conway, T.J.; Doney, S.C.; Feely, R.A.; Foster, P.; et al. Trends in the sources and sinks of carbon dioxide. Nat. Geosci. 2009, 2, 831–836.
  3. Zeebe, R.E.; Zachos, J.C.; Caldeira, K.; Tyrrell, T. OCEANS: Carbon emissions and acidification. Science 2008, 321, 51–52.
  4. Masson-Delmotte, V.; Zhai, P.; Pörtner, H.-O.; Roberts, D.; Skea, J.; Shukla, P.R.; Pirani, A.; Moufouma-Okia, W.; Péan, C.; Pidcock, R.; et al. (Eds.) IPCC 2018 Summary for Policymakers. In Global Warming of 1.5 °C; An IPCC Special Report on the impacts of global warming of 1.5°C above pre-industrial levels and related global greenhouse gas emission pathways, in the context of strengthening the global response to the threat of climate change, sustainable development, and efforts to eradicate poverty; World Meteorological Organization: Geneva, Switzerland, 2018; 32p., Available online: https://www.ipcc.ch/site/assets/uploads/sites/2/2019/05/SR15_SPM_version_report_LR.pdf (accessed on 23 March 2022).
  5. Doney, S.C.; Fabry, V.J.; Feely, R.A.; Kleypas, J.A. Ocean acidification: The other CO2 problem. Ann. Rev. Mar. Sci. 2009, 1, 169–192.
  6. Caldeira, K.; Wickett, M.E. Anthropogenic carbon and ocean pH. Nature 2003, 425, 365.
  7. Orr, J.C.; Fabry, V.J.; Aumont, O.; Bopp, L.; Doney, S.C.; Feely, R.A.; Gnanadesikan, A.; Gruber, N.; Ishida, A.; Joos, F.; et al. Anthropogenic ocean acidification over the twenty-first century and its impact on calcifying organisms. Nature 2005, 437, 681–686.
  8. Raven, J.; Caldeira, K.; Elderfield, H.; Hoegh-Guldberg, O.; Liss, P.; Riebesell, U.; Shepherd, J.; Turley, C.; Watson, A. Ocean Acidification Due to Increasing Atmospheric Carbon Dioxide; The Royal Society: London, UK, 2005; ISBN 0-85403-617-2.
  9. Hu, M.; Tseng, Y.-C.; Su, Y.-H.; Lein, E.; Lee, H.-G.; Lee, J.-R.; Dupont, S.; Stumpp, M. Variability in larval gut pH regulation defines sensitivity to ocean acidification in six species of the Ambulacraria superphylum. Proc. R. Soc. B Biol. Sci. 2017, 284, 20171066.
  10. Chan, K.Y.K.; Grunbaum, D.; O’Donnell, M.J. Effects of ocean-acidification-induced morphological changes on larval swimming and feeding. J. Exp. Biol. 2011, 214, 3857–3867.
  11. Couturier, C.S.; Stecyk, J.A.W.; Rummer, J.L.; Munday, P.L.; Nilsson, G.E. Species-specific effects of near-future CO2 on the respiratory performance of two tropical prey fish and their predator. Comp. Biochem. Physiol.-A Mol. Integr. Physiol. 2013, 166, 482–489.
  12. Spady, B.L.; Nay, T.J.; Rummer, J.L.; Munday, P.L.; Watson, S.-A. Aerobic performance of two tropical cephalopod species unaltered by prolonged exposure to projected future carbon dioxide levels. Conserv. Physiol. 2019, 7, coz024.
  13. Range, P.; Chícharo, M.A.; Ben-Hamadou, R.; Piló, D.; Fernandez-Reiriz, M.J.; Labarta, U.; Marin, M.G.; Bressan, M.; Matozzo, V.; Chinellato, A.; et al. Impacts of CO2-induced seawater acidification on coastal Mediterranean bivalves and interactions with other climatic stressors. Reg. Environ. Chang. 2014, 14, 19–30.
  14. Ries, J.B.; Cohen, A.L.; McCorkle, D.C. Marine calcifiers exhibit mixed responses to CO2-induced ocean acidification. Geology 2009, 37, 1131–1134.
  15. Wang, M.; Jeong, C.B.; Lee, Y.H.; Lee, J.S. Effects of ocean acidification on copepods. Aquat. Toxicol. 2018, 196, 17–24.
  16. Yamada, Y.; Ikeda, T. Acute toxicity of lowered pH to some oceanic zooplankton. Plankt. Biol. Ecol. 1999, 46, 62–67.
  17. McClintock, J.B.; Amsler, M.O.; Angus, R.A.; Challener, R.C.; Schram, J.B.; Amsler, C.D.; Mah, C.L.; Cuce, J.; Baker, B.J. The Mg-calcite composition of Antarctic echinoderms: Important implications for predicting the impacts of ocean acidification. J. Geol. 2011, 119, 457–466.
  18. Dupont, S.; Dorey, N.; Thorndyke, M. What meta-analysis can tell us about vulnerability of marine biodiversity to ocean acidification? Estuar. Coast. Shelf Sci. 2010, 89, 182–185.
  19. Wootton, J.T.; Pfister, C.A.; Forester, J.D. Dynamic patterns and ecological impacts of declining ocean pH in a high-resolution multi-year dataset. Proc. Natl. Acad. Sci. USA 2008, 105, 18848–18853.
  20. Moschino, V.; Marin, M.G. Spermiotoxicity and embryotoxicity of triphenyltin in the sea urchin Paracentrotus lividus Lmk. Appl. Organomet. Chem. 2002, 16, 175–181.
  21. Bellas, J.; Granmo, Å.; Beiras, R. Embryotoxicity of the antifouling biocide zinc pyrithione to sea urchin (Paracentrotus lividus) and mussel (Mytilus edulis). Mar. Pollut. Bull. 2005, 50, 1382–1385.
  22. Bellas, J.; Fernández, N.; Lorenzo, I.; Beiras, R. Integrative assessment of coastal pollution in a Ría coastal system (Galicia, NW Spain): Correspondence between sediment chemistry and toxicity. Chemosphere 2008, 72, 826–835.
  23. Smith, A.M.; Clark, D.E.; Lamare, M.D.; Winter, D.J.; Byrne, M. Risk and resilience: Variations in magnesium in echinoid skeletal calcite. Mar. Ecol. Prog. Ser. 2016, 561, 1–16.
  24. Chave, K.E. Aspects of the Biogeochemistry of Magnesium 1. Calcareous Marine Organisms. J. Geol. 1954, 62, 266–283.
  25. Andersson, A.J.; Mackenzie, F.T.; Bates, N.R. Life on the margin: Implications of ocean acidification on Mg-calcite, high latitude and cold-water marine calcifiers. Mar. Ecol. Prog. Ser. 2008, 373, 265–273.
  26. Lebrato, M.; McClintock, J.B.; Amsler, M.O.; Ries, J.B.; Egilsdottir, H.; Lamare, M.; Amsler, C.D.; Challener, R.C.; Schram, J.B.; Mah, C.L.; et al. From the Arctic to the Antarctic: The major, minor, and trace elemental composition of echinoderm skeletons. Ecology 2013, 94, 1434.
  27. Anand, M.; Rangesh, K.; Maruthupandy, M.; Jayanthi, G.; Rajeswari, B.; Priya, R.J. Effect of CO2 driven ocean acidification on calcification, physiology and ovarian cells of tropical sea urchin Salmacis virgulata—A microcosm approach. Heliyon 2021, 7, e05970.
  28. Holtmann, W.C.; Stumpp, M.; Gutowska, M.A.; Syré, S.; Himmerkus, N.; Melzner, F.; Bleich, M. Maintenance of coelomic fluid pH in sea urchins exposed to elevated CO2: The role of body cavity epithelia and stereom dissolution. Mar. Biol. 2013, 160, 2631–2645.
  29. Byrne, M.; Smith, A.M.; West, S.; Collard, M.; Dubois, P.; Graba-landry, A.; Dworjanyn, S.A. Warming Influences Mg2+ Content, While Warming and Acidification Influence Calcification and Test Strength of a Sea Urchin. Environ. Sci. Technol. 2014, 48, 12620–12627.
  30. Bray, L.; Pancucci-Papadopulou, M.A.; Hall-Spencer, J.M. Sea urchin response to rising pCO2 shows ocean acidification may fundamentally alter the chemistry of marine skeletons. Mediterr. Mar. Sci. 2014, 15, 510–519.
  31. Di Giglio, S.; Spatafora, D.; Milazzo, M.; M’Zoudi, S.; Zito, F.; Dubois, P.; Costa, C. Are control of extracellular acid-base balance and regulation of skeleton genes linked to resistance to ocean acidification in adult sea urchins? Sci. Total Environ. 2020, 720, 137443.
  32. Uthicke, S.; Liddy, M.; Nguyen, H.D.; Byrne, M. Interactive effects of near-future temperature increase and ocean acidification on physiology and gonad development in adult Pacific sea urchin, Echinometra sp. A. Coral Reefs 2014, 33, 831–845.
  33. Shetye, S.S.; Naik, H.; Kurian, S.; Shenoy, D.; Kuniyil, N.; Fernandes, M.; Hussain, A. pH variability off Goa (eastern Arabian Sea) and the response of sea urchin to ocean acidification scenarios. Mar. Ecol. 2020, 41, 1–11.
  34. Dery, A.; Collard, M.; Dubois, P. Ocean Acidification Reduces Spine Mechanical Strength in Euechinoid but Not in Cidaroid Sea Urchins. Environ. Sci. Technol. 2017, 51, 3640–3648.
  35. Emerson, C.E.; Reinardy, H.C.; Bates, N.R.; Bodnar, A.G. Ocean acidification impacts spine integrity but not regenerative capacity of spines and tube feet in adult sea urchins. R. Soc. Open Sci. 2017, 4, 170140.
  36. Cohen-Rengifo, M.; Agüera, A.; Bouma, T.; M’Zoudi, S.; Flammang, P.; Dubois, P. Ocean warming and acidification alter the behavioral response to flow of the sea urchin Paracentrotus lividus. Ecol. Evol. 2019, 9, 12128–12143.
  37. Mos, B.; Byrne, M.; Dworjanyn, S.A. Biogenic acidification reduces sea urchin gonad growth and increases susceptibility of aquaculture to ocean acidification. Mar. Environ. Res. 2016, 113, 39–48.
  38. Wolfe, K.; Dworjanyn, S.A.; Byrne, M. Effects of ocean warming and acidification on survival, growth and skeletal development in the early benthic juvenile sea urchin (Heliocidaris erythrogramma). Glob. Chang. Biol. 2013, 19, 2698–2707.
  39. Moulin, L.; Grosjean, P.; Leblud, J.; Batigny, A.; Dubois, P. Impact of elevated pCO2 on acid–base regulation of the sea urchin Echinometra mathaei and its relation to resistance to ocean acidification: A study in mesocosms. J. Exp. Mar. Bio. Ecol. 2014, 457, 97–104.
  40. Moulin, L.; Grosjean, P.; Leblud, J.; Batigny, A.; Collard, M.; Dubois, P. Long-term mesocosms study of the effects of ocean acidification on growth and physiology of the sea urchin Echinometra mathaei. Mar. Environ. Res. 2015, 103, 103–114.
  41. Uthicke, S.; Ebert, T.; Liddy, M.; Johansson, C.; Fabricius, K.E.; Lamare, M. Echinometra sea urchins acclimatized to elevated pCO2 at volcanic vents outperform those under present-day pCO2 conditions. Glob. Chang. Biol. 2016, 22, 2451–2461.
  42. Migliaccio, O.; Pinsino, A.; Maffioli, E.; Smith, A.M.; Agnisola, C.; Matranga, V.; Nonnis, S.; Tedeschi, G.; Byrne, M.; Gambi, M.C.; et al. Living in future ocean acidification, physiological adaptive responses of the immune system of sea urchins resident at a CO2 vent system. Sci. Total Environ. 2019, 672, 938–950.
  43. Collard, M.; Rastrick, S.P.S.; Calosi, P.; Demolder, Y.; Dille, J.; Findlay, H.S.; Hall-Spencer, J.M.; Milazzo, M.; Moulin, L.; Widdicombe, S.; et al. The impact of ocean acidification and warming on the skeletal mechanical properties of the sea urchin Paracentrotus lividus from laboratory and field observations. ICES J. Mar. Sci. 2016, 73, 727–738.
  44. Wood, H.L.; Spicer, J.I.; Widdicombe, S. Ocean acidification may increase calcification rates, but at a cost. Proc. R. Soc. B Biol. Sci. 2008, 275, 1767–1773.
  45. Long, W.C.; Swiney, K.M.; Foy, R.J. Effects of ocean acidification on the embryos and larvae of red king crab, Paralithodes camtschaticus. Mar. Pollut. Bull. 2013, 69, 38–47.
  46. Melzner, F.; Gutowska, M.A.; Langenbuch, M.; Dupont, S.; Lucassen, M.; Thorndyke, M.C.; Bleich, M.; Pörtner, H.O. Physiological basis for high CO2 tolerance in marine ectothermic animals: Pre-adaptation through lifestyle and ontogeny? Biogeosciences 2009, 6, 2313–2331.
  47. Kaniewska, P.; Campbell, P.R.; Kline, D.I.; Rodriguez-Lanetty, M.; Miller, D.J.; Dove, S.; Hoegh-Guldberg, O. Major cellular and physiological impacts of ocean acidification on a reef building coral. PLoS ONE 2012, 7, e34659.
  48. Heuer, R.M.; Grosell, M. Physiological impacts of elevated carbon dioxide and ocean acidification on fish. Am. J. Physiol. Integr. Comp. Physiol. 2014, 307, R1061–R1084.
  49. Pörtner, H. Ecosystem effects of ocean acidification in times of ocean warming: A physiologist’s view. Mar. Ecol. Prog. Ser. 2008, 373, 203–217.
  50. Pörtner, H.O.; Bock, C.; Reipschläger, A. Modulation of the cost of pHi regulation during metabolic depression: A 31P-NMR study in invertebrate (Sipunculus nudus) isolated muscle. J. Exp. Biol. 2000, 203, 2417–2428.
  51. Reipschläger, A.; Pörtner, H.O. Metabolic depression during environmental stress: The role of extracellular versus intracellular pH in Sipunculus nudus. J. Exp. Biol. 1996, 199, 1801–1807.
  52. Langenbuch, M.; Bock, C.; Leibfritz, D.; Pörtner, H.O. Effects of environmental hypercapnia on animal physiology: A 13C NMR study of protein synthesis rates in the marine invertebrate Sipunculus nudus. Comp. Biochem. Physiol. Part A Mol. Integr. Physiol. 2006, 144, 479–484.
  53. Carey, N.; Harianto, J.; Byrne, M. Sea urchins in a high-CO2 world: Partitioned effects of body size, ocean warming and acidification on metabolic rate. J. Exp. Biol. 2016, 219, 1178–1186.
  54. Brockington, S.; Peck, L. Seasonality of respiration and ammonium excretion in the Antarctic echinoid Sterechinus neumayeri. Mar. Ecol. Prog. Ser. 2001, 219, 159–168.
  55. Catarino, A.I.; Bauwens, M.; Dubois, P. Acid-base balance and metabolic response of the sea urchin Paracentrotus lividus to different seawater pH and temperatures. Environ. Sci. Pollut. Res. 2012, 19, 2344–2353.
  56. Stumpp, M.; Trübenbach, K.; Brennecke, D.; Hu, M.Y.; Melzner, F. Resource allocation and extracellular acid-base status in the sea urchin Strongylocentrotus droebachiensis in response to CO2 induced seawater acidification. Aquat. Toxicol. 2012, 110–111, 194–207.
  57. Sun, T.; Tang, X.; Jiang, Y.; Wang, Y. Seawater acidification induced immune function changes of haemocytes in Mytilus edulis: A comparative study of CO2 and HCl enrichment. Sci. Rep. 2017, 7, 1–10.
  58. Marčeta, T.; Matozzo, V.; Alban, S.; Badocco, D.; Pastore, P.; Marin, M.G. Do males and females respond differently to ocean acidification? An experimental study with the sea urchin Paracentrotus lividus. Environ. Sci. Pollut. Res. 2020, 27, 39516–39530.
  59. Lewis, C.; Ellis, R.P.; Vernon, E.; Elliot, K.; Newbatt, S.; Wilson, R.W. Ocean acidification increases copper toxicity differentially in two key marine invertebrates with distinct acid-base responses. Sci. Rep. 2016, 6, 1–10.
  60. Collard, M.; Dery, A.; Dehairs, F.; Dubois, P. Euechinoidea and Cidaroidea respond differently to ocean acidification. Comp. Biochem. Physiol.-Part A Mol. Integr. Physiol. 2014, 174, 45–55.
  61. Rich, W.A.; Schubert, N.; Schläpfer, N.; Carvalho, V.F.; Horta, A.C.L.; Horta, P.A. Physiological and biochemical responses of a coralline alga and a sea urchin to climate change: Implications for herbivory. Mar. Environ. Res. 2018, 142, 100–107.
  62. Lawrence, J.M.; Lane, J.M. The utilization of nutrients by post-metamorphic echinoderms. In Echinoderm Nutrition; Jangoux, M., Lawrence, J.M., Eds.; CRC Press: London, UK, 2020; pp. 331–371.
  63. Shick, J.M. Respiratory Gas Exchange in Echinoderms. In Echinoderm Studies; Jangoux, M., Lawrence, J.M., Eds.; CRC Press: Boca Raton, FL, USA, 2020; pp. 67–110.
  64. Cattano, C.; Claudet, J.; Domenici, P.; Milazzo, M. Living in a high CO2 world: A global meta-analysis shows multiple trait-mediated fish responses to ocean acidification. Ecol. Monogr. 2018, 88, 320–335.
  65. Havenhand, J.N.; Buttler, F.-R.; Thorndyke, M.C.; Williamson, J.E. Near-future levels of ocean acidification reduce fertilization success in a sea urchin. Curr. Biol. 2008, 18, R651–R652.
  66. Beniash, E.; Ivanina, A.; Lieb, N.S.; Kurochkin, I.; Sokolova, I.M. Elevated level of carbon dioxide affects metabolism and shell formation in oysters Crassostrea virginica. Mar. Ecol. Prog. Ser. 2010, 419, 95–108.
  67. Mayzaud, P. Respiration and nitrogen excretion of zooplankton. II. Studies of the metabolic characteristics of starved animals. Mar. Biol. 1973, 21, 19–28.
  68. Bayne, B.L.; Widdows, J.; Thompson, T.J. Physiological integrations. In Marine Mussels: Their Ecology and Physiology; Cambridge University Press: Cambridge, UK, 1976; pp. 121–206.
  69. Bayne, B.L.; Brown, D.A.; Burns, K.; Dixon, D.R.; Ivanovici, A.; Livingstone, D.R.; Lowe, D.M.; Moore, M.N.; Stebbing, A.R.D.; Widdows, J. The Effects of Stress and Pollution on Marine Animals; Praeger: Westport, CT, USA, 1985; ISBN 0030570190.
  70. Wang, G.; Yagi, M.; Yin, R.; Lu, W.; Ishimatsu, A. Effects of elevated seawater CO2 on feed intake, oxygen consumption and morphology of Aristotle’s lantern in the sea urchin Anthocidaris crassispina. J. Mar. Sci. Technol. 2013, 21, 192–200.
  71. Asnicar, D.; Novoa-Abelleira, A.; Minichino, R.; Badocco, D.; Pastore, P.; Finos, L.; Munari, M.; Marin, M.G. When site matters: Metabolic and behavioural responses of adult sea urchins from different environments during long-term exposure to seawater acidification. Mar. Environ. Res. 2021, 169, 105372.
  72. Morley, S.A.; Suckling, C.C.; Clark, M.S.; Cross, E.L.; Peck, L.S. Long-term effects of altered pH and temperature on the feeding energetics of the Antarctic sea urchin, Sterechinus neumayeri. Biodiversity 2016, 17, 34–45.
  73. Burnham, K.A.; Nowicki, R.J.; Hall, E.R.; Pi, J.; Page, H.N. Effects of ocean acidification on the performance and interaction of fleshy macroalgae and a grazing sea urchin. J. Exp. Mar. Bio. Ecol. 2022, 547, 151662.
  74. Taylor, J.R.; Lovera, C.; Whaling, P.J.; Buck, K.R.; Pane, E.F.; Barry, J.P. Physiological effects of environmental acidification in the deep-sea urchin Strongylocentrotus fragilis. Biogeosciences 2014, 11, 1413–1423.
  75. Kurihara, H.; Yin, R.; Nishihara, G.N.G.; Soyano, K.; Ishimatsu, A. Effect of ocean acidification on growth, gonad development and physiology of the sea urchin Hemicentrotus pulcherrimus. Aquat. Biol. 2013, 18, 281–292.
  76. Leite Figueiredo, D.A.; Branco, P.C.; dos Santos, D.A.; Emerenciano, A.K.; Iunes, R.S.; Shimada Borges, J.C.; Machado Cunha da Silva, J.R. Ocean acidification affects parameters of immune response and extracellular pH in tropical sea urchins Lytechinus variegatus and Echinometra luccunter. Aquat. Toxicol. 2016, 180, 84–94.
  77. Dupont, S.; Thorndyke, M. Relationship between CO2-driven changes in extracellular acid-base balance and cellular immune response in two polar echinoderm species. J. Exp. Mar. Bio. Ecol. 2012, 424–425, 32–37.
  78. Clements, J.C.; Hunt, H.L. Marine animal behaviour in a high CO2 ocean. Mar. Ecol. Prog. Ser. 2015, 536, 259–279.
  79. Clements, J.C.; Poirier, L.A.; Pérez, F.F.; Comeau, L.A.; Babarro, J.M.F. Behavioural responses to predators in Mediterranean mussels (Mytilus galloprovincialis) are unaffected by elevated pCO2. Mar. Environ. Res. 2020, 161, 105148.
  80. Clements, J.C.; Darrow, E.S. Eating in an acidifying ocean: A quantitative review of elevated CO2 effects on the feeding rates of calcifying marine invertebrates. Hydrobiologia 2018, 820, 1–21.
  81. Watson, S.A.; Lefevre, S.; McCormick, M.I.; Domenici, P.; Nilsson, G.E.; Munday, P.L. Marine mollusc predator-escape behaviour altered by near-future carbon dioxide levels. Proc. R. Soc. B Biol. Sci. 2013, 281.
  82. Nilsson, G.E.; Dixson, D.L.; Domenici, P.; McCormick, M.I.; Sørensen, C.; Watson, S.-A.; Munday, P.L. Near-future carbon dioxide levels alter fish behaviour by interfering with neurotransmitter function. Nat. Clim. Chang. 2012, 2, 201–204.
  83. Clements, J.C.; Sundin, J.; Clark, T.D.; Jutfelt, F. Meta-analysis reveals an extreme “decline effect” in the impacts of ocean acidification on fish behavior. PLoS Biol. 2022, 20, e3001511.
  84. Persons, M.H.; Walker, S.E.; Rypstra, A.L.; Marshall, S.D. Wolf spider predator avoidance tactics and survival in the presence of diet-associated predator cues (Araneae: Lycosidae). Anim. Behav. 2001, 61, 43–51.
  85. Weis, J.S.; Smith, G.; Zhou, T.; Santiago-Bass, C.; Weis, P. Effects of contaminants on behavior: Biochemical mechanisms and ecological consequences. Bioscience 2001, 51, 209–217.
  86. Zhao, C.; Bao, Z.; Chang, Y. Fitness-related consequences shed light on the mechanisms of covering and sheltering behaviors in the sea urchin Glyptocidaris crenularis. Mar. Ecol. 2016, 37, 998–1007.
  87. Barry, J.P.; Lovera, C.; Buck, K.R.; Peltzer, E.T.; Taylor, J.R.; Walz, P.; Whaling, P.J.; Brewer, P.G. Use of a free ocean CO2 enrichment (FOCE) system to evaluate the effects of ocean acidification on the foraging behavior of a deep-sea urchin. Environ. Sci. Technol. 2014, 48, 9890–9897.
  88. Borell, E.M.; Steinke, M.; Fine, M. Direct and indirect effects of high pCO2 on algal grazing by coral reef herbivores from the Gulf of Aqaba (Red Sea). Coral Reefs 2013, 32, 937–947.
  89. Campbell, J.E.; Craft, J.D.; Muehllehner, N.; Langdon, C.; Paul, V.J. Responses of calcifying algae (Halimeda spp.) to ocean acidification: Implications for herbivores. Mar. Ecol. Prog. Ser. 2014, 514, 43–56.
  90. Percy, J.A. Thermal adaptation in the boreo-arctic echinoid Strongylocentrotus droebachiensis (Müller, 1776). II. Seasonal acclimatization and urchin activity. Physiol. Zool. 1973, 46, 129–138.
  91. Bayed, A.; Quiniou, F.; Benrha, A.; Guillou, M. The Paracentrotus lividus populations from the northern Moroccan Atlantic coast: Growth, reproduction and health condition. J. Mar. Biol. Assoc. UK 2005, 85, 999–1007.
  92. Lawrence, J.M.; Cowell, B.C. The righting response as an indication of stress in Stichaster striatus (Echinodermata, asteroidea). Mar. Freshw. Behav. Physiol. 1996, 27, 239–248.
  93. Verling, E.; Crook, A.C.; Barnes, D.K.A. Covering behaviour in Paracentrotus lividus: Is light important? Mar. Biol. 2002, 140, 391–396.
  94. Boudouresque, C.F.; Verlaque, M. Paracentrotus lividus. In Sea Urchins: Biology and Ecology; Lawrence, J.M., Ed.; Elsevier B.V.: Amsterdam, The Netherlands, 2020; pp. 447–485.
  95. Brothers, C.J.; McClintock, J.B. The effects of climate-induced elevated seawater temperature on the covering behavior, righting response, and Aristotle’s lantern reflex of the sea urchin Lytechinus variegatus. J. Exp. Mar. Bio. Ecol. 2015, 467, 33–38.
  96. Pinna, S.; Pais, A.; Campus, P.; Sechi, N.; Ceccherelli, G. Habitat preferences of the sea urchin Paracentrotus lividus. Mar. Ecol. Prog. Ser. 2012, 445, 173–180.
  97. Dumont, C.P.; Drolet, D.; Deschênes, I.; Himmelman, J.H. Multiple factors explain the covering behaviour in the green sea urchin, Strongylocentrotus droebachiensis. Anim. Behav. 2007, 73, 979–986.
  98. Farina, S.; Tomas, F.; Prado, P.; Romero, J.; Alcoverro, T. Seagrass meadow structure alters interactions between the sea urchin Paracentrotus lividus and its predators. Mar. Ecol. Prog. Ser. 2009, 377, 131–137.
  99. Ziegenhorn, M.A. Sea urchin covering behavior: A comparative review. In Sea Urchin—From Environment to Aquaculture and Biomedicine; InTech: London, UK, 2017.
  100. Richner, H.; Milinski, M. On the functional significance of masking behaviour in sea urchins—An experiment with Paracentrotus lividus. Mar. Ecol. Prog. Ser. 2000, 205, 307–308.
  101. Asnaghi, V.; Chindris, A.; Leggieri, F.; Scolamacchia, M.; Brundu, G.; Guala, I.; Loi, B.; Chiantore, M.; Farina, S. Decreased pH impairs sea urchin resistance to predatory fish: A combined laboratory-field study to understand the fate of top-down processes in future oceans. Mar. Environ. Res. 2020, 162, 105194.
  102. Zhao, C.; Ding, J.; Yang, M.; Shi, D.; Yin, D.; Hu, F.; Sun, J.; Chi, X.; Zhang, L.; Chang, Y. Transcriptomes reveal genes involved in covering and sheltering behaviors of the sea urchin Strongylocentrotus intermedius exposed to UV-B radiation. Ecotoxicol. Environ. Saf. 2019, 167, 236–241.
  103. Zhang, L.; Zhang, L.; Shi, D.; Wei, J.; Chang, Y.; Zhao, C. Effects of long-term elevated temperature on covering, sheltering and righting behaviors of the sea urchin Strongylocentrotus intermedius. PeerJ 2017, 5, e3122.
  104. Chi, X.; Sun, J.; Yu, Y.; Luo, J.; Zhao, B.; Han, F.; Chang, Y.; Zhao, C. Fitness benefits and costs of shelters to the sea urchin Glyptocidaris crenularis. PeerJ 2020, 8, e8886.
  105. Nasuchon, N.; Hirasaka, K.; Yamaguchi, K.; Okada, J.; Ishimatsu, A. Effects of elevated carbon dioxide on contraction force and proteome composition of sea urchin tube feet. Comp. Biochem. Physiol. Part D Genom. Proteom. 2017, 21, 10–16.
  106. Dell’Acqua, O.; Ferrando, S.; Chiantore, M.; Asnaghi, V. The impact of ocean acidification on the gonads of three key Antarctic benthic macroinvertebrates. Aquat. Toxicol. 2019, 210, 19–29.
  107. Dupont, S.; Dorey, N.; Stumpp, M.; Melzner, F.; Thorndyke, M. Long-term and trans-life-cycle effects of exposure to ocean acidification in the green sea urchin Strongylocentrotus droebachiensis. Mar. Biol. 2013, 160, 1835–1843.
  108. Hazan, Y.; Wangensteen, O.S.; Fine, M. Tough as a rock-boring urchin: Adult Echinometra sp. EE from the Red Sea show high resistance to ocean acidification over long-term exposures. Mar. Biol. 2014, 161, 2531–2545.
  109. Dworjanyn, S.A.; Byrne, M. Impacts of ocean acidification on sea urchin growth across the juvenile to mature adult life-stage transition is mitigated by warming. Proc. R. Soc. B Biol. Sci. 2018, 285, 20172684.
  110. Kroeker, K.J.; Kordas, R.L.; Crim, R.N.; Singh, G.G. Meta-analysis reveals negative yet variable effects of ocean acidification on marine organisms. Ecol. Lett. 2010, 13, 1419–1434.
  111. Birkhead, T.; Møller, A. Sperm Competition and Sexual Selection; Academic Press Inc.: New York, NY, USA, 1998.
  112. Parker, G.A. Sperm competition and its evolutionary consequences in the insects. Biol. Rev. 1970, 45, 525–567.
More
© Text is available under the terms and conditions of the Creative Commons Attribution (CC BY) license; additional terms may apply. By using this site, you agree to the Terms and Conditions and Privacy Policy.
This entry is offline, you can click here to edit this entry!
ScholarVision Creations
Feedback